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The Didymo Story: the Role of Low Dissolved Phosphorus in the Formation of Didymosphenia Geminata Blooms MAX L

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The Didymo Story: the Role of Low Dissolved Phosphorus in the Formation of Didymosphenia Geminata Blooms MAX L Diatom Research, 2014 Vol. 29, No. 3, 229–236, http://dx.doi.org/10.1080/0269249X.2014.889041 The Didymo story: the role of low dissolved phosphorus in the formation of Didymosphenia geminata blooms MAX L. BOTHWELL1∗, BRAD W. TAYLOR2,3 & CATHY KILROY4 1Environment Canada, Pacific Biological Station, Nanaimo, British Columbia, Canada 2Dept of Biological Sciences, Dartmouth College, Hanover, New Hampshire, USA 3Rocky Mountain Biological Laboratory, Crested Butte, Colorado, USA 4National Institute of Water and Atmospheric Research Ltd., Christchurch, New Zealand We outline, in chronological sequence, the events and findings over 25 years that have shaped our understanding of Didymosphenia geminata (Lyngbye) M. Schmidt blooms. Starting with the first appearance of D. geminata mats in streams on Vancouver Island in the late 1980s and followed years later by blooms in Iceland, South Dakota and Poland, D. geminata blooms were enigmatic for nearly 20 years. Early papers exploring whether blooms were caused by environmental change consistently failed to identify any specific factor(s) associated with their onset. Following the D. geminata outbreak in New Zealand in 2004 that seemed to result from an introduction of the species, the possibility that blooms that had previously occurred elsewhere in the world might also be explained by the introduction and movement among watersheds of a new variant with a bloom-forming tendency was touted and widely accepted. Now, however, the identification of very low soluble reactive phosphorus (SRP; below ∼2 ppb) as the proximate cause of bloom formation, has led to the more likely explanation that D. geminata blooms are the result of large-scale human intervention in climatic, atmospheric and edaphic processes that favour this ultra-oligotrophic species. In this new view, blooms of D. geminata are not simply due to the introduction of cells into new areas. Rather, bloom formation occurs when the SRP concentration is low, or is reduced to low levels by the process of oligotrophication. Mechanisms that potentially cause oligotrophication on global and regional scales are identified. Keywords: river diatom blooms, rock snot, Didymo, phosphorus limitation, global change, atmospheric N-deposition, N-enrichment of landscapes, dissolved phosphorus The early years (1988–1998) of D. geminata-affected rivers on Vancouver Island were Modern episodes of Didymosphenia geminata (Lyngbye) taken during site visits (Fig. 1) and included on an M. Schmidt blooms in rivers were first systematically doc- early website describing the blooms (http://www.env.gov. umented on Vancouver Island, British Columbia in the late bc.ca/wat/wq/didy_bcstrms.html). 1980s (Sherbot & Bothwell 1993, Bothwell et al. 2009). Didymosphenia geminata is native to British Columbia, British Columbia Ministry of Environment (BCMoE) offi- as established by some of the earliest published records cials conducting routine water-quality monitoring in rivers of this species (Lord 1866, Cleve 1894–1896). Because downstream of municipalities in 1988 noticed patchy accu- D. geminata was a native species, a pressing question in the mulations of slimy looking material covering rocks in the 1980s was whether the blooms on Vancouver Island were Heber River, upstream of the town of Gold River. One year new events, or simply newly reported. Because the dense later, several kilometres of the Heber River were covered in benthic mats were occurring in more remote, sparsely pop- Downloaded by [Vermont Fish and Wildlife] at 10:39 18 December 2014 heavy mats. Microscopic examination of the mats revealed ulated areas of the island, this was not an easy question to the stalk-producing diatom D. geminata. The appearance address. Personal testimonies and scientific grey literature of thick algal mats was unusual because the Heber River, were evaluated. For example, mute evidence was avail- like most rivers on Vancouver Island, is nutrient-poor and able in the writings of Roderick Haig-Brown (1908–1976) extensive algal accumulations upstream of known human (Fig. 2). Widely recognized as the 20th century’s finest and nutrient inputs were unprecedented. most prolific angler writer, Haig-Brown lived on Vancou- In 1993, an ad hoc group of biologists and chemists ver Island most of his adult life and was a pioneering river (M. Clark, R. Nordin, J. Deniseger, L. Erikson and C. conservationist. He fished Vancouver Island’s rivers and Wightman) from the BCMoE was established to exam- wrote about them for four decades. In Fisherman’s Fall ine the blooms and determine their causes. Photographs Haig-Brown (1964) describes two of his favourite rivers, ∗Corresponding author. E-mail: [email protected] (Received 5 September 2013; accepted 20 January 2014) © 2014 Copyright of the Crown in Canada. Published by Taylor & Francis. This is an Open Access article. Non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly attributed, cited, and is not altered, transformed, or built upon in any way, is permitted. The moral rights of the named author(s) have been asserted. 230 Bothwell et al. Fig. 2. Roderick Haig-Brown (1908–1976). A pioneer river conservationist, prolific author and resident fly fisherman of Van- couver Island for 42 years. No mention of nuisance benthic algal mats occurs in his writings. (Reproduced with permission of the Haig-Brown Institute.) Fig. 1. The British Columbia Didymosphenia ad hoc group viewing the D. geminata bloom in the Englishman River in 1993. In the late 1970s, Fisheries and Oceans Canada con- ducted a study of the impact of nutrients discharged by the Heber and the Stamp, in both of which D. geminata fish hatcheries into rivers in British Columbia by quanti- blooms were documented in the 1990s. If these blooms had fying algal biomass and diatom species abundance (Munro occurred in his lifetime, Haig-Brown would most likely et al. 1985). The Puntledge River on Vancouver Island was have seen them and written about them, but no mention included in this study. Between 1978 and 1980, D. geminata appears in his works. was never sufficiently abundant to make the list of quan- The weakness of Haig-Brown’s testimony is that tifiable diatom taxa, although it was occasionally present Downloaded by [Vermont Fish and Wildlife] at 10:39 18 December 2014 absence of evidence is not evidence of absence. For this (Munro et al. 1985). Starting in 1991 and continuing to reason, confirmation from long-time observers of Vancou- the present, D. geminata accumulations persist in varying ver Island rivers was sought. In 1976, the Fish and Wildlife degrees in the Puntledge River. Munro et al. (1985) cor- Branch of BCMoE engaged a team of professional fish- roborate that D. geminata was present in Vancouver Island eries biologists as a Steelhead Snorkel Survey Team (SSST) rivers prior to 1989, but in low abundance. to conduct annual censuses of steelhead escapement in The most likely factors for increased benthic algae in response to diminishing returns to Vancouver Island rivers. streams are typically either eutrophication (i.e., increased For 13 years, the SSST annually snorkel-surveyed the cali- concentration of nutrients, most often phosphorus) or brated reaches of many rivers and filed reports on steelhead declines in the intensity of physical disturbance or scour numbers. Starting in the early 1990s, the team noted that (Biggs & Close 1989, Biggs 2000). In 1993, we exam- benthic surfaces were being covered with thick brown ined water chemistry (BCMoE Environmental Monitoring mucilaginous mats that had not occurred in the preceding System Web Reporting) and hydrological (Water Survey of decade (L. Carswell, G. Horncastle, R. Hooton, R. Axford Canada, HYDAT 1992) databases for rivers on Vancouver and S. Hay, pers. commun.). Notes from the SSST helped Island. Although the analysis was hampered by a 3 ppb min- document the development of D. geminata proliferations imum detection limit for SRP, there was no indication that among rivers on Vancouver Island. the onset of blooms resulted from either an increase in SRP The Didymo story 231 or benign hydrological conditions (Sherbot & Bothwell exists (James et al. 2013). Although greater solar exposure 1993). can increase D. geminata stalk length (Kilroy & Bothwell In the 1990s, ground level increases in solar ultraviolet 2011a) and has been associated with greater bloom devel- radiation (UVR) resulting from global ozone depletion were opment (James et al. 2013), it appears that the UVR portion identified as a potential threat to aquatic ecosystems at mid of the solar spectrum does not play a major role in D. gemi- and higher latitudes (Häder & Worrest 1991). Unshaded, nata blooms (Kilroy & Bothwell 2011b, Kilroy & Bothwell shallow, clear water streams were especially vulnerable 2014). (Bothwell et al. 1994). Although the inhibition of attached The net result of investigating D. geminata blooms on riverine diatom communities by natural UVR was signifi- Vancouver Island in the early years was that, although cant, of most relevance was the finding that some species it was a native species, the blooms appeared to be a of stalked diatoms in the genera Gomphoneis and Cymbella new phenomenon, and there was no obvious change in appeared to be preferentially favoured under exposure to environmental conditions that might explain them. UV light (Bothwell et al. 1993). Didymosphenia geminata, however, was not found in the experiment. A later, in situ, experiment was run in 1995 to assess On the boots of fishermen the deleterious effects of UVR on aquatic insects (Kelly The onset of D. geminata blooms in New Zealand in 2004 2001). During a 70-day experiment, diatom samples were was widely attributed to the incursion of a new species collected and enumerated, but at the time, the data were (Kilroy 2004). This suggestion reignited questions about not analysed. We recently analysed the Kelly data. Two- the cause of blooms on Vancouver Island 15 years previ- way analysis of variance (ANOVA) revealed no consistent ously.
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